The cell wall binding domain of Listeria bacteriophage endolysin PlyP35 recognizes terminal GlcNAc residues in cell wall teichoic acid

Molecular Microbiology

Volumn 81, Issue 6, 2011, Pages 1419-1432

  Eugster, Marcel R ^a   Haug, Martina C ^a   Huwiler, Simona G ^a   Loessner, Martin J ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BACTERIOPHAGE ENDOLYSIN PLYP35; CARBOHYDRATE; CELL WALL BINDING DOMAIN P35; N ACETYLGLUCOSAMINE; PEPTIDOGLYCAN; POLYRIBITOL PHOSPHATE; RECOMBINANT PROTEIN; TEICHOIC ACID; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; CONTROLLED STUDY; GENE DELETION; GENE INACTIVATION; GENETIC COMPLEMENTATION; GLYCOSYLATION; IMO2549 GENE; IMO2550 GENE; LISTERIA MONOCYTOGENES; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION;

ACETYLGLUCOSAMINE; AMINO ACID SEQUENCE; BACTERIOPHAGES; CELL WALL; DNA MUTATIONAL ANALYSIS; ENDOPEPTIDASES; LISTERIA MONOCYTOGENES; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; TEICHOIC ACIDS; VIRAL PROTEINS;

BACTERIA (MICROORGANISMS); LISTERIA; LISTERIA MONOCYTOGENES;

EID: 80052741109     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07774.x     Document Type: Article

References (54)

1. Akbar, S., and Price, C.W. (1996) Isolation and characterization of csbB, a gene controlled by Bacillus subtilis general stress transcription factor sigma B. Gene 177: 123-128.
2. Autret, N., Dubail, I., Trieu-Cuot, P., Berche, P., and Charbit, A. (2001) Identification of new genes involved in the virulence of Listeria monocytogenes by signature-tagged transposon mutagenesis. Infect Immun 69: 2054-2065.
3. Borysowski, J., Weber-Dabrowska, B., and Gorski, A. (2006) Bacteriophage endolysins as a novel class of antibacterial agents. Exp Biol Med (Maywood) 231: 366-377.
4. Coligan, J.E., Kindt, T.J., and Krause, R.M. (1978) Structure of the streptococcal groups A, A-variant and C carbohydrates. Immunochemistry 15: 755-760.
5. Endl, J., Seidl, H.P., Fiedler, F., and Schleifer, K.H. (1983) Chemical composition and structure of cell wall teichoic acids of staphylococci. Arch Microbiol 135: 215-223.
6. Eugster, M.R., and Loessner, M.J. (2011) Rapid analysis of Listeria monocytogenes cell wall teichoic acid carbohydrates by ESI-MS/MS. PLoS ONE 6: e21500.
7. Ferretti, J.J., McShan, W.M., Ajdic, D., Savic, D.J., Savic, G., Lyon, K., etal. (2001) Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci USA 98: 4658-4663.
8. Fiedler, F. (1988) Biochemistry of the cell surface of Listeria strains: a locating general view. Infection 16 (Suppl. 2): S92-S97.
9. Fiedler, F., and Ruhland, G.J. (1987) Structure of Listeria monocytogenes Cell Walls. Bull Inst Pasteur 85: 287-300.
10. Fiedler, F., Schäffler, M.J., and Stackebrandt, E. (1981) Biochemical and Nucleic Acid Hybridisation Studies on Brevibacterium linens and Related Strains. Arch Microbiol 129: 85-93.
11. Fiedler, F., Seger, J., Schrettenbrunner, A., and Seeliger, H.P.R. (1984) The Biochemistry of Murein and Cell-Wall Teichoic-Acids in the Genus Listeria. Syst Appl Microbiol 5: 360-376.
12. Fischetti, V.A. (2005) Bacteriophage lytic enzymes: novel anti-infectives. Trends Microbiol 13: 491-496.
13. Fujii, H., Kamisango, K., Nagaoka, M., Uchikawa, K., Sekikawa, I., Yamamoto, K., and Azuma, I. (1985) Structural study on teichoic acids of Listeria monocytogenes types 4a and 4d. J Biochem (Tokyo) 97: 883-891.
14. Garcia, E., Garcia, J.L., Garcia, P., Arraras, A., Sanchez-Puelles, J.M., and Lopez, R. (1988) Molecular evolution of lytic enzymes of Streptococcus pneumoniae and its bacteriophages. Proc Natl Acad Sci USA 85: 914-918.
15. Gill, S.C., and von Hippel, P.H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182: 319-326.
16. Glaser, L., and Burger, M.M. (1964) The Synthesis of Teichoic Acids. 3. Glucosylation of Polyglycerophosphate. J Biol Chem 239: 3187-3191.
17. Glaser, P., Frangeul, L., Buchrieser, C., Rusniok, C., Amend, A., Baquero, F., etal. (2001) Comparative genomics of Listeria species. Science 294: 849-852.
18. Gorski, L. (2008) Phenotypic Identification. In Handbook of Listeria Monocytogenes. Liu, D. (ed.). Boca Raton: Taylor & Francis CRC Press, pp. 139-168.
19. Hermoso, J.A., Monterroso, B., Albert, A., Galan, B., Ahrazem, O., Garcia, P., etal. (2003) Structural basis for selective recognition of pneumococcal cell wall by modular endolysin from phage Cp-1. Structure 11: 1239-1249.
20. Hermoso, J.A., Garcia, J.L., and Garcia, P. (2007) Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Curr Opin Microbiol 10: 461-472.
21. Horton, R.M., Hunt, H.D., Ho, S.N., Pullen, J.K., and Pease, L.R. (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68.
22. Hu, S., Kong, J., Kong, W., Guo, T., and Ji, M. (2010) Characterization of a novel LysM domain from Lactobacillus fermentum bacteriophage endolysin and its use as an anchor to display heterologous proteins on the surfaces of lactic acid bacteria. Appl Environ Microbiol 76: 2410-2418.
23. Huang, X., and Helmann, J.D. (1998) Identification of target promoters for the Bacillus subtilis sigma X factor using a consensus-directed search. J Mol Biol 279: 165-173.
24. Kamisango, K., Fujii, H., Okumura, H., Saiki, I., Araki, Y., Yamamura, Y., and Azuma, I. (1983) Structural and immunochemical studies of teichoic acid of Listeria monocytogenes. J Biochem (Tokyo) 93: 1401-1409.
25. Kaya, S., Araki, Y., and Ito, E. (1985) Structural studies on the linkage unit between poly(galactosylglycerol phosphate) and peptidoglycan in cell walls of Bacillus coagulans. Eur J Biochem 147: 41-46.
26. Kojima, N., Araki, Y., and Ito, E. (1983) Structure of linkage region between ribitol teichoic acid and peptidoglycan in cell walls of Staphylococcus aureus H. J Biol Chem 258: 9043-9045.
27. Korndörfer, I.P., Danzer, J., Schmelcher, M., Zimmer, M., Skerra, A., and Loessner, M.J. (2006) The crystal structure of the bacteriophage PSA endolysin reveals a unique fold responsible for specific recognition of Listeria cell walls. J Mol Biol 364: 678-689.
28. Kretzer, J.W., Lehmann, R., Schmelcher, M., Banz, M., Kim, K.P., Korn, C., and Loessner, M.J. (2007) Use of high-affinity cell wall-binding domains of bacteriophage endolysins for immobilization and separation of bacterial cells. Appl Environ Microbiol 73: 1992-2000.
29. Lauer, P., Chow, M.Y., Loessner, M.J., Portnoy, D.A., and Calendar, R. (2002) Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J Bacteriol 184: 4177-4186.
30. Lei, X.H., Fiedler, F., Lan, Z., and Kathariou, S. (2001) A novel serotype-specific gene cassette (gltA-gltB) is required for expression of teichoic acid-associated surface antigens in Listeria monocytogenes of serotype 4b. J Bacteriol 183: 1133-1139.
31. Lipkin, D., Phillips, B.E., and Abrell, J.W. (1969) Action of hydrogen fluoride on nucleotides and other esters of phosphorus(V) acids. J Org Chem 34: 1539-1547.
32. Loessner, M.J. (2005) Bacteriophage endolysins - current state of research and applications. Curr Opin Microbiol 8: 480-487.
33. Loessner, M.J., Wendlinger, G., and Scherer, S. (1995) Heterogeneous endolysins in Listeria monocytogenes bacteriophages: a new class of enzymes and evidence for conserved holin genes within the siphoviral lysis cassettes. Mol Microbiol 16: 1231-1241.
34. Loessner, M.J., Schneider, A., and Scherer, S. (1996) Modified Listeria bacteriophage lysin genes (ply) allow efficient overexpression and one-step purification of biochemically active fusion proteins. Appl Environ Microbiol 62: 3057-3060.
35. Loessner, M.J., Kramer, K., Ebel, F., and Scherer, S. (2002) C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Mol Microbiol 44: 335-349.
36. Mavris, M., Manning, P.A., and Morona, R. (1997) Mechanism of bacteriophage SfII-mediated serotype conversion in Shigella flexneri. Mol Microbiol 26: 939-950.
37. Navarre, W.W., Ton-That, H., Faull, K.F., and Schneewind, O. (1999) Multiple enzymatic activities of the murein hydrolase from staphylococcal phage phi11. Identification of a d-alanyl-glycine endopeptidase activity. J Biol Chem 274: 15847-15856.
38. Park, S.F., and Stewart, G.S. (1990) High-efficiency transformation of Listeria monocytogenes by electroporation of penicillin-treated cells. Gene 94: 129-132.
39. Promadej, N., Fiedler, F., Cossart, P., Dramsi, S., and Kathariou, S. (1999) Cell wall teichoic acid glycosylation in Listeria monocytogenes serotype 4b requires gtcA, a novel, serogroup-specific gene. J Bacteriol 181: 418-425.
40. Sambrook, J., and Russel, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
41. Sanderson, A.R., Strominger, J.L., and Nathenson, S.G. (1962) Chemical structure of teichoic acid from Staphylococcus aureus, strain Copenhagen. J Biol Chem 237: 3603-3613.
42. Schleifer, K.H., and Kandler, O. (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36: 407-477.
43. Schmelcher, M., Shabarova, T., Eugster, M.R., Eichenseher, F., Tchang, V.S., Banz, M., and Loessner, M.J. (2010) Rapid multiplex detection and differentiation of Listeria cells using fluorescent phage endolysin cell wall binding domains. Appl Environ Microbiol 76: 5745-5756.
44. Schmelcher, M., Tchang, V.S., and Loessner, M.J. (2011) Domain shuffling and module engineering of Listeria phage endolysins for enhanced lytic activity and binding affinity. Microb Biotechnol doi: 10.1111/j.1751-7915.2011.00263.x.
45. Seeliger, H.P.R., and Höhne, K. (1979) Serotyping of Listeria monocytogenes and related species. In Methods in Microbiology. Bergan, T., and Norris, J. (eds). New York: Academic Press, pp. 31-49.
46. Smith, K., and Youngman, P. (1992) Use of a new integrational vector to investigate compartment-specific expression of the Bacillus subtilis spoIIM gene. Biochimie 74: 705-711.
47. Spears, P.A., Suyemoto, M.M., Palermo, A.M., Horton, J.R., Hamrick, T.S., Havell, E.A., and Orndorff, P.E. (2008) A Listeria monocytogenes Mutant Defective in Bacteriophage Attachment is Attenuated in Orally Inoculated Mice and Impaired in Enterocyte Intracellular Growth. Infect Immun 76: 4046-4054.
48. Uchikawa, K., Sekikawa, I., and Azuma, I. (1986) Structural studies on teichoic acids in cell walls of several serotypes of Listeria monocytogenes. J Biochem (Tokyo) 99: 315-327.
49. Valyasevi, R., Sandine, W.E., and Geller, B.L. (1990) The bacteriophage kh receptor of Lactococcus lactis subsp. cremoris KH is the rhamnose of the extracellular wall polysaccharide. Appl Environ Microbiol 56: 1882-1889.
50. Vinogradov, E., Sadovskaya, I., Li, J., and Jabbouri, S. (2006) Structural elucidation of the extracellular and cell-wall teichoic acids of Staphylococcus aureus MN8m, a biofilm forming strain. Carbohydr Res 341: 738-743.
51. Wang, I.N., Smith, D.L., and Young, R. (2000) Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol 54: 799-825.
52. Wendlinger, G., Loessner, M.J., and Scherer, S. (1996) Bacteriophage receptors on Listeria monocytogenes cells are the N-acetylglucosamine and rhamnose substituents of teichoic acids or the peptidoglycan itself. Microbiology 142: 985-992.
53. Young, R. (1992) Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56: 430-481.
54. Zimmer, M., Sattelberger, E., Inman, R.B., Calendar, R., and Loessner, M.J. (2003) Genome and proteome of Listeria monocytogenes phage PSA: an unusual case for programmed + 1 translational frameshifting in structural protein synthesis. Mol Microbiol 50: 303-317.